Date of Award

Spring 1-1-2025

Document Type

Dissertation

Degree Name

Doctor of Philosophy (PhD)

Department

Physics

First Advisor

Murrell, Michael

Abstract

Active matter is a subfield of soft condensed matter physics that focuses on the emergence ofcollective phenomena, as components of the system consume energy, driving them out of thermodynamic equilibrium. Living matter, a specific subfield of active matter, lies between physics and biology. In this case, the components are biomolecules, whose interactions are not only constrained by the laws of physics but may exhibit purpose and intentionality. Biophysicists, who study living matter use reductionist approaches and focus on how different components of the system can collectively give rise to novel biological phenomena through continuous consumption of energy. An example of a driven, non-equilibrium thermodynamic system is the cell cytoskeleton, which is an exquisite machinery that is responsible for complex tasks such as migration and division. It is composed of proteins and other biological macromolecules which interact to yield collective behaviors. For example, the protein scaffolding of the cell (F-actin) undergoes dramatic changes in structure, organization, and dynamics through impartation of mechanical stresses by molecular motors (myosin) which consume chemical energy during these morphological changes. However, how the consumption of chemical energy drives the mechanical performance of biological, protein-based machines is unknown. By using cutting edge biophysical experimental techniques and tools such as confocal microscopy, (micro)rheology, and pico-calorimetry, this thesis examines phenomena across scales from molecular level energetic consumption and dissipation to large micrometer-level collective and critical phenomena. We use the bottom-up approach and assemble the biomimetic cytoskeletal structure, the actomyosin network, using minimalistic purified protein components (in vitro). In this thesis, I will summarize several aspects related to the active mechanics and energetics of the cytoskeletal assembly such as how material properties relate to chemical consumption and vice versa. In doing so, I will describe unique aspects of non-equilibrium materials, including active stress propagation, energy consumption and dissipation, self-tuned critical behaviors, novel constitutive relationships, emergence of spatiotemporal instabilities (in vitro actin waves), and the change in heat dissipation and energetic efficiency. From these findings, we offer novel insights on the cytoskeleton as an auto-feedback network system that uses mechanochemical and biomechanical cues to regulate mechanical information propagation as well as the bioenergetic properties of the cytoskeleton as a crucial part of the machinery. We challenge the current understanding of the cytoskeleton field from a more network- focused perspective and motivate the investigation of how a cell regulates its energetic efficiency as an out-of-equilibrium thermodynamical machine.

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